Journal of

Plankton Research academic.oup.com/plankt

J. Plankton Res. (2021) 1–15. doi:10.1093/plankt/fbab008

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BLOOFINZ - Gulf of Mexico
Mesozooplankton biomass, grazing
and trophic structure in the bluefin
tuna spawning area of the oceanic Gulf
of Mexico
MICHAEL R. LANDRY* AND RASMUS SWALETHORP
scripps institution of oceanography, university of california, san diego, 9500 gilman dr., la jolla, ca 92093-0227, usa

*corresponding author: mlandry@ucsd.edu

Received October 13, 2020; editorial decision January 13, 2021; accepted February 1, 2021

Corresponding editor: Xabier Irigoyen

We investigated size-fractioned biomass, isotopes and grazing of mesozooplankton communities in the larval habitat
of Atlantic bluefin tuna (ABT) in the oceanic Gulf of Mexico (GoM) during the peak spawning month of May.
Euphotic-zone biomass ranged from 101 to 513 mg C m−2 during the day and 216 to 798 mg C m−2 at
night. Grazing varied from 0.1 to 1.0 mg Chla m−2 d−1 , averaging 1–3% of phytoplankton Chla consumed d−1 .
Carnivorous taxa dominated the biomass of > 1-mm zooplankton (78% day; 60% night), while only 13% of
smaller zooplankton were carnivores. δ 15 N enrichment between small and large sizes indicates a 0.5–0.6 trophic-
step difference. Although characteristics of GoM zooplankton are generally similar to those of remote oligotrophic
subtropical regions, zooplankton stocks in the ABT larval habitat are disproportionately high relative to primary
production, compared with HOT and BATS averages. Growth-grazing balances for phytoplankton were resolved
with a statistically insignificant residual, and trophic fluxes from local productivity were sufficient to satisfy C demand
of suspension feeding mesozooplankton. While carnivore C demand was met by local processes in the central GoM,
experiments closer to the coastal margin suggest the need for a lateral subsidy of zooplankton biomass to the oceanic
region.

KEYWORDS: zooplankton; biomass; subtropical; oligotrophic; growth-grazing balance; production; carbon

demand; suspension feeders; carnivores; migrants; active export

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 JOURNAL OF PLANKTON RESEARCH VOLUME 00
INTRODUCTION
The central role of mesozooplankton as trophic inter-
mediaries between primary producers and fish is well
recognized in the classic paradigm of marine food webs
(Hardy, 1924) and in studies of larval fish ecology, where
the temporal matching of prey resources to the needs
of larvae in seasonally dynamic environments is often
viewed as a critical determinant of recruitment success
(Hjort, 1914; Cushing, 1990). In less dynamic larval nurs-
ery areas, such as oligotrophic subtropical waters, rela-
tionships between fish larvae and zooplankton prey are
likely just as important, though more subtle and nuanced
(Llopiz et al., 2014; Landry et al., 2019). For example, like
many tuna and billfish species, Atlantic bluefin tuna (ABT,
Thunnus thynnus) spawn in nutritionally dilute subtropical
waters rather than in more-productive adjacent coastal
margins as an apparent tradeoff between larval starvation
and predation risks (Bakun and Broad, 2003; Bakun,
2013; Shropshire et al., this issue). Further complicating
interpretation of this strategy, however, ABT larvae are
concentrated in fronts and eddies rather than randomly
distributed (Bakun, 2006, 2013; Alemany et al., 2010; Lin-
do-Atichati et al., 2012), suggesting that specific properties
of mesoscale habitats might matter more to larval success
than temporal dynamics or mean open-ocean conditions.
Extensive sampling of ABT larvae in the Gulf of Mex-
ico (GoM) since the 1970s has defined narrow environ-
mental windows in which ABT can be found in oceanic
waters of the GoM, as well as their particular prevalence
in the outer rings of anticyclonic loop eddies that spin off
periodically from the Loop Current (Muhling et al., 2010,
2011; Lindo-Atichati et al., 2012). Domingues et al. (2016)
linked these relationships to satellite measurements of
seasurface height and temperature, establishing a dimen-
sionless index that both successfully captured the general
features of larval spatial distributions and temporal vari-
ability in the GoM and also explained 58% of interannual
stock recruitment variability over a two-decade period
(1993–2011). The trophic ecology of ABT larval habit,
however, is entirely unexplored. Coherent plankton food-
web studies have not been done in any oceanic waters of
the GoM, and there are no prior estimates of mesozoo-
plankton carbon biomass or community grazing in the
region. The present study thus addresses a void in basic
knowledge of regional ecology while also contributing to
a broader system-level process investigation of ABT larval
habitat in the oceanic GoM (Gerard et al., this issue).
As part of the BLOOFINZ-GoM project (Bluefin
Larvae in Oligotrophic Ocean Foodwebs, Investigation
of Nitrogen to Zooplankton in the GoM), we investi-
gated biomass and grazing rates of mesozooplankton
communities in ABT larval habitat in 2017 and 2018
2
NUMBER 00 PAGES 1–15 2021
during the peak spawning month of May. The use of
similar methodology allows us compare zooplankton and
environmental characteristics in the GoM to those at
oligotrophic subtropical sites in the Atlantic and Pacific
Oceans that have been systematically studied for decades,
and to process studies in other warm-water open-ocean
systems. We further draw upon results from companion
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studies of phytoplankton production (Yingling et al., this
issue) and phytoplankton growth and microzooplankton
grazing (Landry et al., this issue) to put zooplankton
biomass and grazing in the context of broader trophic
fluxes. From these, we address the questions: How much
does mesozooplankton grazing contribute to the balance
of phytoplankton growth rate and fates in GoM larval
ABT habitat? Are trophic fluxes in these waters sufficient
to satisfy the carbon demands of actively growing
zooplankton? What are the relative magnitudes of trophic
flows to mesozooplankton in these areas?
METHODS
Zooplankton sample collection
Mesozooplankton samples were taken in offshore olig-
otrophic waters of the GoM during BLOOFINZ-GoM
cruises NF1704 (7 May–2 June 2017) and NF1802
(27 April–20 May 2018) on NOAA Ship Nancy Foster.
Sampling was guided by the habitat index model of
Domingues et al. (2016) based on real-time satellite
imagery (Gerard et al., this issue). Over the two cruises,
five quasi-Lagrangian process studies, hereafter “cycles”
C1–C5, of 2–4-day duration were conducted following
the paths of a satellite-tracked drifter with a mixed-
layer drogue (Fig. 1; Landry et al., 2009). Substantial
abundances of ABT larvae were found in mixed-layer
(upper 25 m) waters during C1 (2017) and C5 (2018)
(Shiroza et al., this issue). During cycle experiments,
we sampled each mid-day (1100–1300) and mid-night
(23:00–01:00) with a 1-m diameter ring net (0.2-mm
Nitex mesh) towed obliquely through the euphotic zone
at a ship speed of ∼1.5 kt. Additional transect samples
(T1 and T2) were taken across frontal features at the
beginning of the 2018 cruise at irregular times of day
(mostly afternoons to evenings between 13:30 and 20:20).
Tow depth was controlled directly by shipboard readout
from a pressure sensor at the point of net attachment
on the hydrowire. Tow distance and volume filtered were
measured with a calibrated General Oceanics flowmeter
(GO, Miami, FL) attached across the net mouth, assuming
100% filtration efficiency. For NF1704, pressure rating of
the hydrowire depth sensor limited net tows to 100-m
depth. For NF1802, mean tow depth was 133 ± 2 m.
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE
Fig. 1. Sampling locations for mesozooplankton day and night net tows
in the GoM. Traces in map inlay depict drift trajectories of Cycles 1–3
in May 2017 and C4–5 in May 2018. Additional transect sampling (T1
and T2) was done in 2018.
Upon retrieval, cod-end contents were anesthetized
with CO2 (ice-cold soda water; Kleppel and Pieper 1984)
to slow metabolism and gut evacuation and immediately
split with a Folsom plankton splitter. Half of the tow was
preserved in borate-buffered 5% formalin. The remain-
ing half was size fractioned by wet sieving through nested
screens of 5, 2, 1, 0.5 and 0.2-mm Nitex mesh to produce
5 size classes of 0.2–0.5, 0.5–1, 1–2, 2–5 and 5+ mm.
Organisms retained on each mesh were concentrated
onto separate pre-weighed filters (47-mm diameter) of
0.2-mm Nitex, rinsed with isotonic ammonium formate
solution to remove interstitial sea salt, then placed in indi-
vidual petri dishes and frozen at −80◦ C for later analysis.
On several occasions, we collected small pyrosomes (5–
8 cm) that were too few to subsample quantitatively. We
removed these prior to splitting and size fractioning and
froze them separately in 50-mL Falcon tubes for weighing
and gut pigment analyses.
Biomass and stable isotope analyses
In the laboratory, frozen size-fractioned zooplankton on
Nitex filters were thawed, set briefly on blotting paper to
remove excess water and weighed moist for total sample
wet weight (WW). Wet samples were subsampled for gut
pigments by removing replicate portions of the biomass
and recording weights before and after each subsampling
(fraction of total WW removed). The remaining wet
biomass on the filters was oven dried at 60◦ C for 24 h
before weighing dry for the dry weight to wet weight
ratio (DW:WW). For each size fraction, zooplankton DW
(mg m−2 ) was calculated from the measured WW (less
initial filter weight), DW:WW ratio, measured volume
3
and depth of tow, and fraction of sample analyzed. The
remaining dried sample was subsequently scraped off the
filter, ground to a powder and subsampled by weight for
carbon (C), nitrogen (N) and stable isotope (13 C and 15 N)
analyses. Individual pyrosomes were treated similarly to
the size-fractioned samples by first measuring total WW
and dividing the WW into subsamples for pigment, DW
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and CN analyses.
CN subsamples were weighed in small tin boats, packed
into pellets, and analyzed by standard elemental analyzer,
isotope ratio mass spectrometry (EA-IRMS) (Owens and
Rees, 1989) at the Isotope Biogeochemistry lab at Scripps
Institution of Oceanography. The continuous flow system
consisted of a Perkin Elmer CHN analyzer coupled to
a Thermo/Finnigan Delta Plus IRMS. Acetanilide was
the standard used for measurement stability on every run.
C and N biomass estimates (mg m−2 ) were computed for
each size fraction from C:DW and N:DW ratios. Stable
isotope values are reported in standard δ () notation
relative to atmospheric N2 and Vienna Pee Dee Belemnite
for carbon.
Gut pigment and grazing estimates
WW subsamples were placed in glass tubes with 7 mL
of 90% acetone and homogenized (multiple 20-s bursts)
in an ice bath with a Vibracell sonicator probe. They
were then extracted overnight (18–24 h) in a −20◦ C
freezer and warmed to room temperature in a dark con-
tainer prior to analysis. The homogenate was shaken and
centrifuged (5 min at 3000 rpm) to remove particulates.
Concentrations of chlorophyll a (Chla) and phaeopig-
ments (Phaeo) were then measured by the acidification
method using a 10-AU fluorometer (Strickland and Par-
sons 1972). Water-column estimates of depth-integrated
Chla for the euphotic zone were made similarly from
analyses of duplicate 0.25 L samples collected from CTD
hydrocasts, extracted for 24 h in 90% acetone, and mea-
sured on the same fluorometer.
For each size-fraction analyzed, we computed the
depth-integrated concentration of gut pigment (Chla,
Phaeo) in the euphotic zone as:
pig∗ D
GPC =
vol∗ f
where GPC is gut pigment content (mg m−2 ), pig is the
measured pigment value (mg), f is fraction of sample
analyzed, D is depth of tow (m) and vol is the volume of
water filtered (m3 ). To be conservative, our zooplankton
grazing estimates are based only on measured gut Phaeo
values, without correction for inefficiencies in converting
Chla into Phaeo.
 JOURNAL OF PLANKTON RESEARCH
We estimated grazing rates (G, mg pigment m−2 time−1 )
for each size fraction and for the total zooplankton assem-
blage as G = GPC ∗ K , where K (min−1 ) is the gut evac-
uation rate constant. For K , we used a gut passage rate
of 2.1 h−1 measured under similar surface water temper-
atures in the equatorial Pacific (Zhang et al., 1995). To
compute carbon-specific rates of phytoplankton grazing
by the zooplankton size classes, we divided G by carbon
biomass (mg C m−2 ). Daily removal rates of phytoplank-
ton by zooplankton grazing were computed as G ∗ Chlz −1 ,
where Chlz is the depth-integrated concentration of Chla
in the euphotic zone (mg Chla m−2 ).
Carnivorous feeders
As a relatively simple index of trophic structure, we
divided the mesozooplankton community into two feed-
ing groups: animals considered to be exclusively carniv-
orous (only consuming other animals) and omnivorous
suspension feeders (mixed feeding on phytoplankton, sus-
pended particles, heterotrophic protists and likely small
developmental stages of other animals). For this, we vol-
umetrically subsampled the formalin-preserved split of
the zooplankton samples with a Stempel pipette after
thorough mixing and size fractioned the sample through
a 1-mm Nitex screen. Except for C2, 2-day and 2-night
tows were subsampled from each cycle. After rinsing with
fresh water, zooplankton taxa in the > 1-mm fraction
were identified under a dissecting microscope and sorted
into carnivores and suspension feeders. Each group was
placed together on pre-weighed Nitex, dried for 24 h at
60◦ C and measured as DW. Percent carnivore was deter-
mined as the fraction of total subsample DW attributable
to carnivorous taxa. For the < 1-mm fraction, we deter-
mined percent carnivore in terms of relative abundances
by dispersing the subsample in a Bogorov sorting tray and
enumerating the first ∼ 275 animals encountered (range
255–316) into the two feeding categories.
Metabolic and growth requirements
To estimate feeding requirements for well-nourished
zooplankton, we calculated expected rates of respiration
and growth from empirical relations based on zooplank-
ton size and environmental temperature. For respiration,
we used the equation of Ikeda (1985):
   
ln Ro μl O2 ind−1 h−1 = 0.8354∗ ln Ci mg C ind−1
 
+0.0601∗ T ◦ C + 0.5254,
where Ci is the average carbon content of an individ-
ual zooplankter in size-fraction i. Potential growth rates
(G, d−1 ) were computed from the equation of Hirst and
VOLUME 00 NUMBER 00 PAGES 1–15 2021
Sheader (1997):
     
log10 G d−1 = −0.2962∗ log10 Ci μg C ind−1 + 0.0246∗ T ◦ C –1.1355.
For both respiration and growth rate equations, we
used mean estimates of individual zooplankton carbon
(2.4, 7.4, 41, 140 and 2 782 μg C ind−1 for the 0.2–0.5 to
5+ mm size fractions, respectively) determined from mea-
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sured size-fractioned abundances and carbon biomass in
144 net tows from the subtropical Pacific (Landry et al.,
2001). Temperature was the mean euphotic-zone value
(T EZ ) in Table I. Respiration rates for each size class were
converted to carbon equivalents using the molar volume
of an ideal gas at standard temperature and pressure
(22.4 L mol−1 ), the respiratory quotient (0.97; Hernán-
dez-León and Ikeda, 2005), and the molecular weight of
carbon (12 g C mol−1 ) and multiplying by zooplankton
abundance (total C biomass/C ind−1 ). Growth rates (d−1 )
were converted to production estimates by multiplying by
C biomass of the zooplankton assemblage (mg C m−2 ) and
averaging day and night estimates at each station. Cal-
culations of ingestion rates (carbon demand) needed to
satisfy respiration and growth requirements also assumed
70% absorption efficiency for ingested food (Steinberg
and Landry, 2017). Estimates of mesozooplankton con-
tribution to carbon export by active diel vertical migra-
tors were similarly calculated from the biomass differ-
ences between paired day and night tows (size-fractioned
migrant biomass) and the mean temperature in the 300–
500-m depth range assuming that migrants spend 12 h
per day in this stratum (Al Mutairi and Landry, 2001).
RESULTS
Environmental conditions
All zooplankton net tows were conducted in warm olig-
otrophic waters with low mixed-layer Chla and prominent
deep chlorophyll maxima (DCM). Mixed-layer depths
(MLD) were generally in the range of 20–35 m but
substantially deeper and more variable for T1 sampling
(56 ± 17 m) and shallowest (12 ± 0.5 m) for C5 (Table I).
DCM depths varied by > 40 m on each cruise but were
22-m shallower, on average, during 2018 compared with
2017 (p < 0.001). Conversely, integrated concentrations
of euphotic-zone Chla were higher in 2018 than in 2017
for all composite sampling locations, and almost double
on average (p < 0.001). While mixed-layer Chla varied
slightly, but significantly for 2017 and 2018 (0.11± 0.01
versus 0.09 ± 0.01 mg Chla m−3 , respectively; p < 0.004),
most of the difference between years was in the lower
euphotic zone, as indicated by larger DCM peak concen-
trations in 2018 (0.71 ± 0.04 versus 0.54 ± 0.04 mg Chla
4
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE

Table I: Environmental conditions for zooplankton net tows in the GoM during May 2017 (Cycles 1–3)
and April–May 2018 (Transects 1–2; Cycles 4–5)
Samples Dates MLD (m) DCM (m) T ML (◦ C) T EZ (◦ C) Chla (mg m−2 )

Cycle 1 11–14 May 31.5 ± 4.0 100 ± 1.3 24.5 ± 0.12 23.6 ± 0.36 17.7 ± 1.0
Cycle 2 16–18 May 24.2 ± 1.1 120 ± 7.9 25.3 ± 0.06 24.4 ± 0.04 16.2 ± 1.4
Cycle 3 27–30 May 25.8 ± 4.1 137 ± 1.7 26.7 ± 0.07 24.8 ± 0.02 13.7 ± 0.7
Trans 1 30 Apr–1 May 56.1 ± 17.2 100 ± 10.8 26.1 ± 0.28 25.2 ± 0.77 35.1 ± 6.7
26.6 ± 0.4 92 ± 4.4 24.9 ± 0.10 24.2 ± 0.49 43.0 ± 0.3

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Trans 2 2 May
Cycle 4 5–9 May 23.7 ± 1.2 111± 7.1 25.6 ± 0.07 24.8 ± 0.05 24.1 ± 1.2
Cycle 5 15–19 May 12.4 ± 0.5 77 ± 3.9 25.5 ± 0.14 24.2 ± 0.22 29.2 ± 5.4
2017 28.1 ± 1.6 118 ± 4.0 25.5 ± 0.23 24.2 ± 0.15 15.8 ± 0.5
2018 26.4 ± 5.0 95 ± 4.6 25.6 ± 0.10 24.5 ± 0.20 29.4 ± 2.3

MLD (m) = mixed layer depth, where seawater density is 0.1 kg m−3 greater than at 10 m. DCM (m) = depth of the Deep Chlorophyll Maximum;
T ML (◦ C) = mean temperature of the mixed layer; T EZ (◦ C) = mean euphotic-zone temperature to the DCM; and CHLZ (mg m−2 ) is mean
depth-integrated Chla to the DCM. 2017 and 2018 cruise are averages for all tows in cruise years. Uncertainties are standard errors of mean
values.
Bold font is used to highlight the averages of cruise years, as opposed to the averages of individual cycle experiments in the two years.

Table II: Carbon (C), nitrogen (N), WW and DW relationships for mesozooplankton size classes in the
oceanic GoM
Size fraction DW:WW (%) C:DW (%) N:DW (%) C:N

0.2–0.5 mm 14.8 ± 0.8 36.8 ± 0.3 8.18 ± 0.09 4.51 ± 0.03

0.5–1 mm 16.5 ± 1.0 39.4 ± 0.3 9.91 ± 0.08 4.28 ± 0.02
1–2 mm 11.6 ± 0.4 38.5 ± 0.3 9.06 ± 0.08 4.25 ± 0.03
2–5 mm 13.4 ± 1.8 35.7 ± 0.4 8.61 ± 0.11 4.15 ± 0.04
5+ mm 8.5 ± 2.0 26.5 ± 1.6 6.21 ± 0.45 4.21 ± 0.16
Total 12.1 ± 0.7 36.0 ± 1.6 8.47 ± 0.14 4.25 ± 0.03

Averages are based on 44 day and nighttime euphotic-zone net tows in May 2017 and May 2018. Uncertainties are standard errors of mean
values.
Bold font is used to highlight the averages of cruise years, as opposed to the averages of individual cycle experiments in the two years.

m−3 ; p < 0.001). Despite the Chla differences, water tem-
peratures varied narrowly ∼24.5–26.5◦ C for the mixed
layer and 23–25◦ C for the euphotic zone and were not
different, on average, between years (p > 0.20).
Elemental and weight relationships
Day-night differences in DW:WW ratios were not
significant for any of the zooplankton size classes
(P > 0.25). In 2017, C:DW was significantly lower at night
(33.4 ± 1.9%) than during the day (38.4 ± 0.6%) due to
more large gelatinous animals in the euphotic zone at
night, which lowered the carbon content of the 5+ mm
size fraction from 30.6 to 19.1% of DW (P < 0.035).
For 2018 and the other 2017 size fractions, day-night
variability in %C:DW was insignificant. Because most
of the variability in elemental and weight conversions
occurs among size classes rather than time of day, we
highlight these differences by averaging all day and night
tows together in Table II.
Carbon is the biomass basis for all subsequent anal-
yses. The C:DW relationship is highest for the 0.5–1
and 1–2 mm fractions (39.4 and 38.5%, respectively)
and decreases significantly in the order of 0.2–0.5 mm
(36.8%; P < 0.001) > 2–5 mm (35.7%; P < 0.05) > 5+
mm (26.5%; P < 0.001; Table II). The C:N ratio for the
0.2–0.5 mm fraction (4.51) is significantly higher than
both of the 1–2 and 2–5 mm fractions (4.25 and 4.15,
respectively; P < 0.0001), while all other size fractions
show no C:N differences. The difference in the small-
est size fraction may reflect some contamination from
large phytoplankton or detritus, which have higher C:N
compositions than zooplankton.
Biomass variability
Mesozooplankton carbon biomass varies substantially in
our analyses among sampling locations (cycles), between
day-night tows, between cruise years and among size
classes (Fig. 2). Among cycles, mean day biomasses
range 5 fold from 101 ± 12 to 513 ± 71 mg C m−2
for C2 and C5, respectively. Nighttime biomasses
range 3.7 fold from 216 ± 16 (C1) to 798 ± 28 (C5)
mg C m−2 . Within years, night tow biomass averages
are significantly higher than day averages in 2017
(239 ± 15 versus 144 ± 16 mg C m−2 ; P < 0.001), but
not in 2018 (514 ± 69 versus 424 ± 53 mg C m−2 ;
P > 0.31). Between years, both day and night biomass

5
 JOURNAL OF PLANKTON RESEARCH VOLUME 00
Fig. 2. Size-fractioned carbon biomass structure of mesozooplankton
in the GoM during Cycles 1–5 drift experiments and total average
carbon for day (D) and night (N) tows in 2017 and 2018 cruises. Totals
for 2018 include T1 and T2 sampling, in addition to C4 and C5.
Uncertainties are standard errors of mean estimates.
averages are significantly higher in 2018 than 2017
for the total (P < 0.002) and for each individual size
fraction in day and night tows (P < 0.02), except for
5+ mm animals during the day (P > 0.40). Among
size classes for all net tows, the 1–2 mm fraction
contributes most to biomass (29.9 ± 1.3%; P < 0.016),
the 0.5–1 and 2–5 mm fractions contribute comparably
(23.7 ± 1.2 and 24.8 ± 1.6%, respectively; P > 0.60),
and further contributions decline in order of 0.2–
0.5 mm (16.5 ± 0.9%; P < 0.001) and 5+ mm fractions
(5.0 ± 0.8%; P < 0.001). For night tows only, inclusive
of diel migrants, the 2–5 and 1–2 mm fractions are
the biomass co-dominants (29.1 ± 2.1 and 27.4 ± 1.7%,
respectively; P > 0.54), and further contributions decline
in order of 0.5–1 mm (22.2 ± 1.6%; P < 0.03), 0.2–
0.5 mm (14.2 ± 1.1%; P < 0.001) and 5+ mm fractions
(7.2 ± 1.2%; P < 0.001).
Grazing rates and size relationships
Mean grazing rate estimates range from 0.1 to 1.0 mg
Chla m−2 d−1 for the whole mesozooplankton community
and show substantial variability among cycles, day and
night tows, years and size classes (Fig. 3). The main dif-
ferences are shaped by the variability in biomass (Fig. 2).
Similar to biomass trends, for example, the lowest and
highest grazing rates are for C2 and C5 (0.22 ± 0.08 and
0.82 ± 0.13 mg Chla m−2 d−1 , respectively; P < 0.004),
and 2018 grazing is higher overall compared with
2017 (0.52 ± 0.08 and 0.33 ± 0.03 mg Chla m−2 d−1 ;
P < 0.025). In contrast to biomass, however, nighttime
grazing estimates do not differ significantly from day
estimates for the full community for either of the 2 years
separately or both years combined (0.48 ± 0.07 versus
0.39 ± 0.06 mg Chla m−2 d−1 , P > 0.38), and only the
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NUMBER 00 PAGES 1–15 2021
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Fig. 3. Size-fractioned grazing of mesozooplankton in the GoM during
Cycles 1–5 drift experiments and average total grazing for day (D) and
night (N) tows in 2017 and 2018 cruises. Uncertainties are standard
errors of mean estimates.
2–5 mm fraction has a marginal difference between night
and day tows (P < 0.048). These departures from the
biomass trends reflect differences among size classes and
cycles in carbon-specific grazing rates (Table III).
Overall, we found no significant differences between
day and night estimates of C-specific grazing for any of
the size fractions (P > 0.05 for 5+ mm; P > 0.21 for all
other sizes) or for the whole community (P > 0.38). C-
specific grazing does, however, vary significantly among
all size classes, as might be expected, in exact inverse
order of mean animal size (Table III, P < 0.03:0.2–
0.5 mm (2.43 ± 0.23μg Chl mg C d−1 ) > 0.5–1 mm
(1.65 ± 0.12 μg Chl mg C d−1 ; P < 0.003) > 1–2 mm
(1.14 ± 0.07 μg Chl mg C d−1 ; P < 0.001) > 2–5 mm
(0.85 ± 0.02 μg Chl mg C d−1 ; P < 0.03) > 5+ mm
(0.05 ± 0.02 μg Chl mg C d−1 ; P < 0.001). Although C-
specific grazing estimates are higher in 2017 than 2018
across all sizes (Table III), the differences are significant
for only the 0.2–0.5 mm (P < 0.004), 2–5 mm (P < 0.016)
and total (P < 0.001) size categories.
Isotopic composition
Day and night tows did not give statistically different
isotopic values for any of the zooplankton size fractions
and are reported as mean values in Fig. 5. δ 15 N also did
not differ among size fractions in the 2 years, but δ 13 C
was 0.3–0.6 lower (P < 0.01) for the smallest 3 frac-
tions (0.2–2 mm) in 2018 compared with 2017. Among
size classes, δ 15 N increases significantly from 0.2–0.5 mm
(3.38 ± 0.19) to 0.5–1 mm (4.05 ± 0.19; P < 0.014)
and to 1–2 mm (4.96 ± 0.22; P < 0.003) zooplankton,
but size fractions > 1 mm have similar values in the range
of 5.0–5.25 (P > 0.35) (Fig. 5A). Assuming that a 3.4
increase in bulk δ 15 N corresponds to one full trophic level
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE
Table III: Carbon-specific grazing rates for size-fractioned mesozooplankton in the GoM during Cycle 1–5
experiments and for all tows in 2017 and 2018 cruises
Carbon-specific grazing rates (μg Chla mg C−1 d−1 )
Samples 0.2–0.5 mm 0.5–1 mm
Cycle 1 2.51 ± 0.22 1.68 ± 0.18
Cycle 2 2.19 ± 0.07 1.45 ± 0.14
Cycle 3 4.25 ± 0.64 2.28 ± 0.17
Cycle 4 1.67 ± 0.32 1.09 ± 0.11
Cycle 5 2.04 ± 0.31 1.84 ± 0.39
2017 3.18 ± 0.35 1.88 ± 0.13
2018 1.86 ± 0.26 1.47 ± 0.17
Uncertainties are standard errors of mean values.
Bold font is used to highlight the averages of cruise years, as opposed to the averages of individual cycle experiments in the two years.
of isotopic enrichment (Minawaga and Wada, 1984), the
1.87 difference between smaller and larger zooplank-
ton size fractions suggests a 0.55 step increase in mean
trophic position.
Despite the slight negative trend, none of the size-
fraction comparisons for δ 13 C are significant (P > 0.35;
Fig. 5B). On average, therefore, zooplankton in the differ-
ent size classes appears to share a common food-web base.
Carnivorous feeders
Among smaller (0.2–1 mm) mesozooplankton, carnivo-
rous taxa comprised a small, but relatively consistent,
fraction of the community (13.1 ± 0.7%) that did not vary
significantly (P > 0.07) between day and night sample
collections (Fig. 5). Copepods of the family Corycaeidae
and small chaetognaths were the main contributors to this
feeding group in the samples examined.
Among larger (>1 mm) zooplankton, carnivorous taxa
dominated euphotic-zone biomass, significantly more
during day (78.4 ± 5.0%) than night tows (60.5 ± 4.5%;
P < 0.013) (Fig. 5). This difference reflects the entry
of diel vertical migrants into the euphotic zone at
night, especially large euphausiids, which we scored
conservatively as omnivorous suspension feeders given
the undocumented feeding status of most species.
Conspicuous taxa comprising the carnivorous group were
abundant large chaetognaths and large copepods of the
genus Euchaeta, most of which appeared to reside in the
euphotic-zone day and night. In addition to euphausiids,
copepods of the genera Neocalanus and Eucalanus were
significant contributors to suspension feeding biomass in
most samples, while salps were relatively small and rare.
This analysis does not account for the pyrosomes removed
from samples prior to splitting, which were few in number
(5 small colonies in 44 tows) and only collected at night.
Considering pyrosomes would therefore have lowered the
nighttime percentage of carnivorous biomass, though not
substantially.
1–2 mm 2–5 mm 5+ mm Total
1.06 ± 0.15 0.85 ± 0.27 — 1.50 ± 0.13
0.81 ± 0.18 1.05 ± 0.45 0.14 ± 0.14 1.22 ± 0.12
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1.53 ± 0.13 1.50 ± 0.33 0.12 ± 0.08 2.06 ± 0.17
0.90 ± 0.09 0.39 ± 0.11 0.06 ± 0.06 0.81 ± 0.11
1.35 ± 0.22 0.88 ± 0.18 0.001 ± 0.001 1.24 ± 0.15
1.20 ± 0.10 1.17 ± 0.20 0.08 ± 0.04 1.67 ± 0.12
1.09 ± 0.10 0.61 ± 0.09 0.03 ± 0.20 1.05 ± 0.09
Carbon demand and migrant export
Because temperature varies little among the sampling
locations (Table I), calculated estimates of mesozooplank-
ton carbon demand (Fig. 6) closely follow biomass vari-
ability (Fig. 2), except that smaller size classes contribute
proportionally more to total C demand because of the
size functions in respiration and growth equations (Ikeda,
1985; Hirst and Sheader, 1997). C demand ranges from
67.5 ± 0.5 to 15.1 ± 0.1% body C d−1 for 0.2–0.5 mm
and 5+ mm size fractions, respectively, and averages
42 ± 0.7% body C d−1 for the community. Day-night
and cruise differences of C demand as % body C d−1
are insignificant. The total feeding required to meet C
demand is, however, significantly higher in 2018 than
2017 (194 ± 17 versus 80 ± 6 mg C m−2 d−1 ; P < 0.001).
The annual averages in Fig. 6 separate portions of
total C demand that can be satisfied by carnivorous
versus omnivorous suspension feeding based on the con-
tributions of those feeding groups to small (0.2–1 mm)
and large (>1 mm) zooplankton in Fig. 5. The propor-
tions of C demand assigned to each feeding group were
partitioned according to average % carnivore for day
and night tows of each cycle (T1 and T2 samples were
portioned according to mean day and night estimates
for C4 and C5 combined), then summed for the total
community and averaged per year. Of the total C demand
for 2017, 29.1 ± 2.1 and 50.4 ± 4.0 mg C m−2 d−1 are
ascribed to carnivores and suspension feeders, respec-
tively. For 2018, C demand divides into 74.9 ± 7.0 and
119.2 ± 10.8 mg C m−2 d−1 for carnivores and suspension
feeders. On average, ∼ 38% of total C demand can be
satisfied by direct predation on metazooplankton.
Mean temperature in the 300–500 m depth stratum
ranged from 10.6 to 12.4◦ C (11.7 ± 0.02◦ C) for the 5
cycles where we had paired day and night tows to com-
pute active export flux by respiration of diel migrants.
Some of the estimates were slightly negative when day
biomass values exceeded nighttime values (range − 3.3 to
7
 JOURNAL OF PLANKTON RESEARCH VOLUME 00
15.6 mg C m−2 d−1 ). The mean active export estimate of
3.7 ± 1.1 mg C m−2 d−1 represents, on average, the daily
respiratory loss of 3.2 ± 0.4% of the body C of migrant
zooplankton.
DISCUSSION
Although we intended to sample consistently in this study
to depths that included the DCM, that was not possible for
all tows on the 2017 cruise. Because DCMs were deepest
for C2 and C3, the samples collected for those cycles
were the most compromised by this issue, with missed
DCM sampling potentially affecting estimates of total
biomass m−2 , day-night differences, relative size structure
and grazing rates relative to water-column Chla. For
example, the daytime biomass estimates for C2 and C3
are the lowest for all tows while nighttime estimates are
comparable or higher than for C1 (Fig. 2). Similarly, day-
time grazing estimates are extremely low for C2, though
not for C3, whereas nighttime grazing for C2 and C3 are
both comparable and higher than C1 and C4 (Fig. 3).
A substantial portion of the zooplankton community
appears to reside in the lower euphotic zone, between
100 m and the DCM, during the day, but comes into
the upper 100 m at night, along with regular migrants
that completely leave the euphotic zone during the day.
Thus, while C2 and C3 euphotic depths were under-
sampled also at night, nighttime biomass and grazing
estimates to 100 m provide more useful comparisons
to other cycles. Based on them, the biomass difference
between years appears to be valid, scaling approximately
with the 2-fold higher concentrations of integrated Chla
in 2018 compared with 2017 (Table I). Grazing, however,
does not scale proportionately with the Chla difference
between years because the C-specific grazing rate for
the zooplankton community was ∼ 60% higher in 2017
(Table III).
Due to the sampling depth irregularities for C2 and C3,
we focus most of the discussion below on C1, C4 and C5,
which are also the better characterized experiments for
phytoplankton growth rates and microzooplankton graz-
ing (Landry et al., this issue), allowing more comprehen-
sive assessments of trophic interactions for these cycles. In
the sections below, we first compare results for the GoM
to other warm-water oceanic regions investigated with
similar methods. We then address the two major questions
of our study. What is the role of mesozooplankton grazing
in the balance of phytoplankton growth and losses in the
GoM? How do various trophic processes contribute to
satisfying mesozooplankton carbon demand?
Comparisons to other open-ocean regions
Despite numerous corrections for net type, mesh size,
tow depth and measurement units, global analyses
8
NUMBER 00 PAGES 1–15 2021
have been useful in defining broad-scale patterns of
zooplankton biomass (Moriarty and O’Brien, 2013;
Moriarty et al., 2013). In general, subtropical waters (15–
40◦ ) are biomass minima between higher zooplankton
stocks in tropical (15◦ S–15◦ N) and temperate-to-high-
latitude (40–90◦ ) waters. We examine the low-latitude,
warm-water component of this pattern in Table IV for a
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subset of studies with methods comparable to the present
study, including time-series sampling in the subtropical
North Pacific (Stn. ALOHA, Hawaii Ocean Time-series,
HOT) and subtropical North Atlantic (Sargasso Sea,
Bermuda Atlantic Time-series Study, BATS) as well as
process studies in the eastern tropical Pacific, equatorial
Pacific and eastern Indian Ocean.
As in the global trend, mesozooplankton biomass is
higher in our subset of studies for tropical regions than
adjacent subtropical systems (Table IV). For example,
biomass in the central equatorial Pacific (994 ± 77 mg C m−2 ;
Décima et al., 2011) is almost three times higher than
the long-term average at Stn. ALOHA in the North
Pacific subtropical gyre (349 ± 26 mg C m−2 ; Valencia
et al., 2018). Biomass in tropical waters of the eastern
Indian Ocean along 110◦ E is also more than double
the average in subtropical Indian Ocean Central Water
directly to the south (455 ± 18 versus 209 ± 32 mg C m−2 ;
Landry et al., 2020a). Similarly, various crossing of
the Atlantic Meridional Transect have documented
substantially higher (1.5-16X) zooplankton biomass in
the equatorial Atlantic than in subtropical gyres of the
North and South Atlantic (Isla et al., 2004; López and
Anadón, 2008; Calbet et al., 2009). Such differences
arise because these tropical systems are associated with
divergence or mixing centers that enhance productivity
relative to the more pervasive downwelling of subtropical
gyres. Nonetheless, as shown in Table IV, this occurs
without much of a difference in total integrated Chla
because the shallow concentrated euphotic zones of
richer systems are compensated for by deeper euphotic
zones with pronounced DCMs in the subtropics. The
importance of relative productivity, rather than latitude,
in driving such differences is illustrated by sampling along
160◦ E in the western Pacific (Sun and Wang, 2017).
In this case, equatorial waters are a local minimum in
mesozooplankton biomass compared with the latitudinal
trend to the north because they reside in a deep layer
of oligotrophic waters, the Western Warm Pool, which
does not allow significant upwelling of nutrients despite
conducive winds.
GoM results are consistent with the lower primary
production and zooplankton biomass expected for
subtropical regions (Table IV). Our mesozooplankton
biomass estimates are almost identical to the long-term
average from the subtropical Pacific at Stn. ALOHA (349
versus 351 mg C m−2 , respectively), though substantially
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE

Table IV: Comparison of environmental conditions, mesozooplankton biomass and grazing estimates
among open-ocean tropical and subtropical regions
T EZ Intgr Chla PrimProd Biomass Grazing
Region Latitude (◦ C) (mg m−2 ) (mg C m−2 d−1 ) (mg C m−2 ) (% Chla d−1 ) Refs

Costa Rica Dome 9–11 ◦N 22.0 ± 0.3 24.1 ± 1.5 1 025 ± 113 1870 ± 72 54 ± 11 1
Equatorial Pacific 4◦ S-4◦ N 24.2 ± 0.2 26.7 ± 0.7 672 ± 3.7 994 ± 77 14 ± 6 2
Tropical E. Indian 11–14◦ S 26.9 ± 0.6 25.7 ± 2.9 ND 455 ± 18 21 ± 4 3
27–35◦ S 19.6 ± 0.4 27.2 ± 3.8 209 ± 32 3 ± 0.4

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Subtrop. E. Indian ND 3
W. Equat. Pac, 160◦ E 5◦ S–10◦ N 30.0 25.5 ND 259 ND 4
Subtrop. N. Pacific 22–23◦ N 24.4 ± 0.1 23.0 ± 0.2 516 ± 11 349 ± 26 ND 5
Subtrop. Atlantic 31–32◦ N 21.3 ± 0.1 24.8 ± 2.4 455 ± 11 218 ± 4 3 to 24 6
Gulf of Mexico 25.4–27◦ N 24.5 ± 0.2 22.8 ± 0.2 325 ± 14 351 ± 33 2 ± 0.2 7

References: (1) Décima et al. (2016), Landry et al. (2016), Taylor et al. (2016); (2) Balch et al. (2011), Décima et al. (2011), Landry et al. (2011),
Taylor et al. (2011); (3) Landry et al. (2020b); (4) Sun and Wang (2017); (5) Hawaii Ocean Time series (HOT), https://hahana.soest.hawaii.edu/hot/
hot-dogs/, Valencia et al. (2018); (6) Bermuda Atlantic Time Series (BATS), http://bats.bios.edu/data/, Madin et al. (2001), Roman et al. (1993); (7)
This study, Selph et al. (in press), Yingling et al. (this issue).
T EZ (◦ C) and Intgr Chla (mg m−2 ) are mean temperature and depth-integrated Chla of the euphotic zone. PrimProd is the measured rate of
daily primary production from 14 C or 13 C-labeled bicarbonate uptake (mg C m−2 d−1 ). Biomass (mg C m−2 ) estimates are for mesozooplankton
collected in oblique tows with 200-μm mesh nets covering the euphotic zone, originally presented as carbon or calculated from DW using a
C:DW ratio of 0.36. Grazing impact estimates are for the percent of total euphotic-zone Chla (phytoplankton) cleared by mesozooplankton per
day. Uncertainties are standard errors of mean values.

higher than the average for BATS in the Sargasso
Sea (218 ± 4 mg C m−2 ). Though sampled similarly,
HOT zooplankton biomass has long been known to
exceed that at BATS (Roman et al., 2002), and they
remain consistently separated even as biomass has
increased by 60–80% in both systems over the past
three decades (Sheridan and Landry, 2004; Steinberg
et al., 2012; Valencia et al., 2016). Although mean
primary production is also higher at Stn. ALOHA (516
versus 455 mg C m−2 d−1 ), the two sites have different
biomass:production ratios of 0.68 (HOT) and 0.48 mg
C (mg C)−1 d−1 (BATS). Paradoxically, relatively high
zooplankton biomass in the GoM is associated with low
primary production (325 mg C m−2 d−1 ; Yingling et al.,
this issue), giving a much higher biomass:production ratio
(1.07 mg C (mg C)−1 d−1 ) than either HOT or BATS. One
explanation for this difference is temporal aliasing, as the
GoM samples were only collected in May of 2 years, while
the time-series station averages are for all months over
many years. May sampling may simply catch a seasonal
imbalance in the magnitude of accumulated zooplankton
relative to contemporaneous primary production. In
addition, since our GoM sampling was site selective,
rather than spatially random, the difference could reflect
unique aspects of the mesoscale features where ABT
larvae are more abundant. Either way, during the ABT
spawning peak in the GoM, the ratio of zooplankton
biomass to primary production in the larval rearing area
is substantially higher than would be predicted from the
averages of well-studied oligotrophic subtropical regions
of the oceans.
Along with the biomass differences, zooplankton graz-
ing impacts on phytoplankton, measured similarly to this
study, are higher in tropical regions (14–54% Chla d−1 )
compared with estimates (2–3% Chla d−1 ) from subtropi-
cal areas. In this regard, the lower estimate of 3% d−1 for
the subtropical Atlantic is from a study by Roman et al.
(1993) that compared zooplankton grazing during stable
stratified conditions (August), which prevail for most of
the year, to the peak of a late-winter overturn event
(March–April), which gave the higher (24% d−1 ) grazing
impact. The phytoplankton bloom that develops from the
upward mixing of deep nutrients is a regular feature of
the seasonal dynamics of the Sargasso Sea that makes
this region more like a tropical upwelling system for a
small portion of the year, as the higher grazing estimate
indicates. The extent to which similar seasonal events
might also occur in the GoM is not known, although the
regular passage of strong tropical storms and hurricanes
through the region in late summer have the potential to
generate strong mixing on local scales (Babin et al., 2004;
Avila-Alonso et al., 2020). At least for May, the region was
strongly stratified and consistent with other subtropical
systems during stratified conditions in showing a relatively
low grazing impact of mesozooplankton.
Several previous studies have commented upon the
relative uniformity of biomass distribution across size
classes < 5 mm in subtropical regions of the Atlantic,
Pacific and Indian Oceans (Landry et al., 2001; Madin
et al., 2001; Valencia et al., 2018; Landry et al., 2020a).
In our GoM samples, however, biomass structure was
tilted to larger sizes, with the 2–5 mm fraction averaging
27% of biomass compared with 16% for 0.2–0.5-mm
animals, whereas these two fractions are similar (20–
23%) in other regions. Larger size classes contribute
more to diel vertical migration. Our estimates of carbon

9
 JOURNAL OF PLANKTON RESEARCH VOLUME 00
respiration at depth by diel migrating zooplankton,
3.7 ± 1.1 mg C m−2 d−1 , are close to comparably
calculated active flux rates for the subtropical Pacific
(3.6 ± 0.4 mg C m−2 d−1 , Al-Mutairi and Landry, 2001;
updated to 4.2 ± 0.2 mg C m−2 d−1 , Valencia et al., 2018)
but substantially higher than estimates for the subtropical
Atlantic (1.2 mg C m−2 d−1 , Steinberg et al., 2000).
Steinberg et al. (2012) updated the earlier migrant flux
estimates for BATS to account for the increase in time-
series biomass but did not separate the carbon respiratory
component from the total active export (4.1 ± 0.3) that
included organic excretion and fecal pellet transport.
Based on the multipliers applied, the updated estimate
for BATS is 60% of that at Stn. ALOHA (Valencia
et al., 2018), so about 2.5 mg C m−2 d−1 for daytime
C respiration at depth. Therefore, consistent with the
differences in total community biomass, the magnitude
of active migrant flux in the oceanic GoM during May
is more like the average for the subtropical North Pacific
than the western subtropical North Atlantic.
Phytoplankton growth and grazing balances
In addition to mesozooplankton grazing rates, measured
daily rate profiles of phytoplankton growth, microzoo-
plankton grazing and net changes in ambient water-
column Chla from dilution experiments during the cycle
experiments (Landry et al., this issue) enable a first-order
analysis of phytoplankton growth rates and fates for the
euphotic zone based on fluorometrically measured Chla
(Table V). C2 is excluded from this analysis because it
was a 2-day experiment with only one resolved rate pro-
file. Depth-integrated estimates of phytoplankton growth
rates range from 0.25 to 0.59 d−1 , and microzooplankton
grazing (0.10–0.42 d−1 ) is the major loss term compared
with mesozooplankton grazing impact (0.01–0.03 d−1 ).
Net change in photic zone Chla varies from a net accumu-
lation rate of +0.16 d−1 for C5 to Chla loss of −0.06 d−1
for C3. None of the water columns investigated was
at steady state. For cycles where we observed net Chla
accumulation in the photic zone (C1, C4 and C5; Landry
et al., this issue), the budgets can be reasonably closed,
between −0.04 and + 0.09 d−1 . Due to the net decline in
Chla during C3, a large portion of that balance (0.16 d−1 )
is unresolved. Thus, for individual cycles, there is mixed
success in reconciling the balance of growth and loss
terms. For the daily resolved rates of all 4 cycles, the
balance residual (0.05 ± 0.04 d−1 ) is equivalent to ∼ 10%
of mean phytoplankton growth rate but is not significantly
greater than zero (t-test, P > 0.11).
Similar analyses have demonstrated tighter bal-
ances of phytoplankton growth rates and fates in the
California Current Ecosystem (Landry et al., 2009),
10
NUMBER 00 PAGES 1–15 2021
equatorial Pacific (Landry et al., 2011) and Costa
Rica Dome (Landry et al., 2016). In the California
Current, measured rates of phytoplankton growth,
microzooplankton grazing and mesozooplankton grazing
explained 93% of the variability in rates of phytoplankton
biomass accumulation along a trophic gradient from
coastal upwelling to oligotrophic open ocean. In the
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equatorial Pacific and Costa Rica Domes, the dynamics
were reflected in steady-state balances of growth and
grazing with low to negligible unresolved residuals. What
these previously studied systems have in common are
phytoplankton concentration maxima in or close to the
mixed layer, therefore in the depth stratum tracked by
drifters with mixed-layer drogues. For the current exper-
iments, Landry et al. (this issue) observed near steady-
state mixed-layer Chla, with microzooplankton grazing
typically equal or exceeding phytoplankton growth, while
growth and grazing were strongly uncoupled in the mid
to lower photic zone, accounting for the net changes in
ambient Chla. Thus, a major challenge in interpreting
growth-grazing balances in the GoM is the large influence
of the portion of the photic zone that shows significant
net biomass rate of change but is not specifically marked
or tracked by the drifter. It is thus difficult to know
whether imbalances for the cycles in Table V are due
to process measurement issues versus lateral inputs that
are not independently measured. Advective influences on
water-column dynamics might also be exacerbated in the
oceanic GoM by strong gradients in the surrounding
coastal margins (Kelly et al., in review) and by our
experimental site selection in mesoscale features. Given
these complications, it may be fortuitous that the process
balances are as well resolved as they appear.
Trophic flows, trophic structure
and carbon demand
Direct grazing on phytoplankton is typically too low to
support full respiration and growth of mesozooplank-
ton in open-ocean ecosystems (Dam et al., 1995; Calbet
et al., 2009). Nonetheless, as recently demonstrated for
the equatorial Pacific (Landry et al., 2020b), the broader
network of trophic flows—including omnivorous feeding
on microzooplankton, carnivory and detritivory—might
still be able to meet the carbon demands of active zoo-
plankton computed from empirical relationships (Fig. 6).
In Table VI, we evaluate this potential for the GoM
for the three experimental cycles with adequate data for
carbon fluxes. Carbon-based estimates of phytoplankton
grazing (7–20 mg C m−2 d−1 ), from daily mean day-night
values of % Chla d−1 cleared by mesozooplankton and
phytoplankton C values for the photic zone (Selph et al.,
in press), account for ∼ 23% of total mesozooplankton C
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE

Table V: Phytoplankton growth rates and fates during cycle process experiments in the GoM
Rate (d−1 ) Cycle 1 Cycle 3 Cycle 4 Cycle 5 ALL

Phyto growth 0.44 ± 0.06 0.37 ± 0.07 0.59 ± 0.05 0.50 ± 0.06 0.49 ± 0.03
Microzoo graz 0.34 ± 0.09 0.24 ± 0.06 0.42 ± 0.09 0.35 ± 0.07 0.34 ± 0.04
Mesozoo graz 0.02 ± 0.004 0.03 ± 0.002 0.01 ± 0.001 0.03 ± 0.002 0.02 ± 0.002
Net change 0.09 ± 0.05 −0.06 ± 0.08 0.06 ± 0.03 0.16 ± 0.09 0.07 ± 0.04
Residual −0.0004 ± 0.01 0.17 ± 0.05 0.09 ± 0.08 −0.04 ± 0.10 0.05 ± 0.04

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Growth-grazing balance residuals are the differences between measured rate estimates for phytoplankton growth and the sum of losses to
micro- and mesozooplankton grazing plus the net rate of biomass change in the euphotic zone during the cycle. All rates are measured by
fluorometric Chla and integrated for the photic zone for daily experiments (Landry et al., this issue). Uncertainties are standard errors of mean
values.
Bold font is used to highlight the averages of cruise years, as opposed to the averages of individual cycle experiments in the two years.

Table VI: Comparisons of nutritional resources relative to mesozooplankton carbon demand for experimen-
tal cycles in the GoM
Variable Cycle 1 Cycle 4 Cycle 5

Nutritional resource (mg C m−2 d−1 )

Phytoplankton grazing 20 ± 6 7±1 20 ± 3
Microzoo production 126 ± 35 116 ± 10 121 ± 10
Mesozoo production 26 ± 3 42 ± 5 77 ± 9
Carbon demand (mg C m−2 d−1 )
Suspension feeders 61 ± 8 91 ± 11 159 ± 24
Carnivorous feeders 27 ± 3 56 ± 8 106 ± 9

Phytoplankton grazing is calculated from % Chla grazed d−1 and phytoplankton C biomass m−2 . Microzoo production is calculated from
the combined C grazing rates of microzooplankton on phytoplankton and bacteria from Landry et al. (this issue), assuming a 30% gross
growth efficiency. Mesozoo Production is computed as described from empirical equations of Hirst and Sheader (1997). Carbon Demands are
computed for suspension feeders and carnivores as described for Fig. 6. All rates are mg C m−2 d−1 . Uncertainties are standard errors of
mean values.

demand for C1 and much lower (5–8%) percentages for
C4 and C5. In comparison, microzooplankton produc-
tion (116–126 mg C m−2 d−1 ), from daily integrated C-
based grazing rates of microzooplankton on phytoplank-
ton and bacteria (Landry et al., this issue) and assuming
a gross growth efficiency of 30% (Straile, 1997), is 6–17
times more important as a potential food resource than
phytoplankton. For C1 and C4, the combined resources
from phytoplankton and microzooplankton substantially
exceed the estimated C demands of suspension feeders.
For C5, the small deficit is within the margin of error
for C demand. While flux distributions would be more
complicated in an actual trophic network, for example
involving small and large microzooplankton and some use
of detritus (Landry et al., 2020b), this simple analysis indi-
cates that trophic flows from locally generated production
in the oceanic GoM in May are adequate to meet the C
demands of suspension feeders, with most coming from
predation on microzooplankton.
From Table VI, the challenge for reconciling trophic
fluxes in the GoM appears to be the availability of
sufficient mesozooplankton production, here calculated
from Hirst and Sheader (1997), to satisfy carnivores.
Mesozooplankton production and carnivore C demand
are balanced for C1, while C4 and C5 have production
deficits of 25–27%. Carnivore C demand could be
overestimated because it derives from a copepod-
based growth relationship (Hirst and Sheader, 1997),
whereas the GoM carnivore biomass is dominated by
chaetognaths. Indeed, the multiple regression equation
developed by Ikeda (2014) for respiration of diverse
zooplankton communities has a negative coefficient,
relative to copepods, for the contribution of chaetognaths
compared with a positive coefficient for euphausiids. For
our samples, overestimates of C demand for chaetognaths
would be offset by underestimates for euphausiids. In
addition, given our very conservative assumption of
no carnivorous feeding by euphausiids and many other
groups, we more likely underestimate total carnivore C
demand. An advective subsidy would be another way to
meet the zooplankton production shortfall.
Kelly et al. (in review) argue for the importance of a
lateral advective organic input from the coastal margins
to explain mass balance deficits of N export in the open-
ocean GoM. Mechanistically, material pulled northward
by the loop current from the productive Campeche Bank
of the Yucatan Peninsula (Merino, 1997; Melo Gonzalez
et al., 2000) could persist as a subsidy in the bodies of
long-lived animals. Studies in the Northern GoM have
also documented evolving dynamics of phytoplankton

11
 JOURNAL OF PLANKTON RESEARCH VOLUME 00 NUMBER 00 PAGES 1–15 2021

and zooplankton during transport in the Mississippi River

plume that leave depleted phytoplankton and a surplus of
zooplankton on the seaward end (Liu and Dagg, 2003;
Liu et al., 2005), where they can be transported into
the oceanic region by eddies. In the present study, back-
tracking of water parcels sampled during our Lagrangian
experiments shows a strong connectivity to the slope

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margin region of the NE GoM several weeks prior to our
sampling for the C1 and C5 experiments with abundant
ABT larvae, but absent that connectivity for cycles C2–
C3 without larvae (Gerard et al., this issue). This suggest
that the NE slope margin may be both a hot spot of
adult spawning activity and a source region of lateral
organic enrichment to the larval ABT rearing habitat. It
may not be coincidental that the cycle (C5, Fig. 1) closest
to this area shows the greatest need for a lateral sub-
sidy of zooplankton to satisfy C demands of carnivores Fig. 4. Bulk d15 N and d13 C isotopic values for mesozooplankton size
while locally generated and balanced trophic fluxes are classes in the GoM. Uncertainties are standard errors of mean estimates.
sufficient to meet C demands of both suspension feeders
and carnivores for water parcel C1 in the central oceanic
GoM. Shropshire et al. (this issue) have further surmised
that a nutritional subsidy from advected zooplankton
may be important for larval ABT survival and point to
the shelf-slope margin as the optimal spawning areas
for minimizing starvation and predation risks of early
larvae.
Dorado et al. (2012) found no difference in δ 13 C val-
ues for zooplankton collected in neritic versus oceanic
waters in the northern GoM (both averaging −19.8 to
−19.9 ± 0.9 SD), despite very substantial δ 13 C differ-
ences in the POM from these two areas. Our similar val-
ues among size classes (Fig. 4) agree with their conclusion
of a common marine-based carbon source for the region.
In terms of trophic structure, the differences in percent
carnivorous feeders between large and small zooplankton Fig. 5. Day and nighttime estimates of percent carnivorous mesozoo-
plankton from net tows done during experimental cycles in the GoM.
are consistent with the inference of a 0.5–0.6 trophic Estimates for the small (<1-mm) size fraction are based on relative
step increase from δ 15 N isotopic enrichment (Figs. 4 and abundances. Estimates for the large (>1-mm) size fraction are based on
5). Despite no difference in δ 13 C, Dorado et al. (2012) relative DW.
reported significantly higher δ 15 N values for neritic versus
oceanic zooplankton (5.5 ± 1.1 and 2.8 ± 1.4, respec-
CONCLUSIONS
tively, for June and July collections), which they attributed
to the lower isotopic values of production from nitrogen Despite a habitat bordered closely by land masses on
fixers in the oceanic region. Our biomass-weighted mean almost all sides, mesozooplankton communities of the
values of δ 15 N from Fig. 4 are in the range of 4.5–4.7, so oceanic GoM exhibit generally similar characteristics to
closer to the previous δ 15 N values for coastal zooplankton. those of remote oligotrophic subtropical regions of the
In addition, nitrogen isotope mass balances for our exper- major oceans in terms of biomass, low grazing impact
imental cycles also revealed very little contribution from on phytoplankton and magnitude of active export from
diazotrophy during the times of our cruises (Knapp et al., respiration by diel migrators. Compared with averages
this issue). If these differences between our results and for HOT and BATS, however, zooplankton stocks are
Dorado et al. (2012) are indicative of a recurrent seasonal disproportionately high relative to contemporaneous pri-
pattern, they suggest a profound and rapid shift up in the mary production in the ABT larval rearing sites during
contribution of N2 fixation to biomass production as the the peak May season. Given the broader context of
ocean warms and further stratifies between May and July. process experiments that measured trophic fluxes and net

12
 LANDRY AND SWALETHORP MESOZOOPLANKTON BIOMASS, GRAZING AND TROPHIC STRUCTURE
Fig. 6. Feeding requirements for mesozooplankton to meet carbon
demands for respiration and production in the GoM during Cycles 1–5
experiments and the average day (D) and night (N) estimates for tows in
2017 and 2018. Yearly averages are divided into feeding requirements
to support suspension feeders (gray-scale shaded, below) and require-
ments to support carnivorous feeders (unshaded, top). Uncertainties are
standard errors of mean cruise estimates for the total community.
biomass changes in the ambient water column, growth-
grazing balances for phytoplankton were resolved with
a slight positive, but statistically insignificant, net resid-
ual, and trophic fluxes generated by local productivity
were found sufficient to satisfy C demand of suspension
feeders. Microzooplankton were the major contributors to
these budgets. Other than the most remote experimental
cycle, C1, which might be a model for how subtropical
ocean regions operate as trophically balanced systems,
experiments conducted closer to the GoM margin show
a zooplankton production deficit, suggesting that lateral
subsidy of zooplankton from the margins is important for
meeting carnivore C demand in the open-ocean region.
DATA ARCHIVING
Data presented here have been submitted to the National
Oceanic and Atmospheric Administration’s (NOAA)
National Centers for Environmental Information (NCEI)
data repository and will also be archived at BCO-
DMO (Biological and Chemical Oceanography Data
Management Office) site https://www.bco-dmo.org/pro
gram/819631.
ACKNOWLEDGEMENTS
We gratefully acknowledge the capable leadership of John
Lamkin and Trika Gerard for the project overall, the cruise
Chief Scientists Estrella Malca (NF1704) and John Lamkin
(NF1802), and the captain and crew of the R/V Nancy Foster.
We additionally thank Sarah Privoznic for her assistance in
organizing the cruises, and Cameron Quackenbush, Juan
Banuelos-Arriaga, Kelsey Fleming and Tabitha Hernandez for
assistance with the field collections and laboratory analyses.
13
FUNDING
This study acknowledges BLOOFINZ-GoM Program support from
National Oceanic and Atmospheric Administration award
NA15OAR4320071 and U.S. National Science Foundation grants
OCE-1756517 and -1851558.
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